The Cotton Mealybug Is Spreading along the Mediterranean: First Pest Detection in Italian Tomatoes

Simple Summary Nowadays, globalization causes a series of negative consequence for the sustainability of agricultural systems, such as solanaceous cultivations. Here, we report for the first time the presence of an invasive polyphagous mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), in Italian solanaceous crops, i.e., tomato and bell pepper. For this, we analyzed at the morphological and molecular level various specimens collected in Sicily during fall 2020. A phylogenetic analysis conducted comparing an ≈800 bp portion of the mitochondrial genome of several worldwide populations, suggests that the introduced population might originate from Asia. This study represents the first step toward establishing a P. solenopsis monitoring and sustainable control program in Europe. Abstract The cotton mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) is an extremely polyphagous invasive pest that can cause serious damages to cultivated plants. The pest is native to America but invaded Asian and Mediterranean countries during the last decades. Tomato (Lycopersicon esculentum Mill., Solanaceae) is an economic relevant crop worldwide and its production can be threatened by numerous insect pests including P. solenopsis. We recorded for the first time P. solenopsis in association with tomato in greenhouse crops and urban landscapes in Sicily (Italy) during the fall season in 2020. The species was identified as P. solenopsis based on the morphological characters and DNA amplification of an ≈800 bp portion of mitochondrial cytochrome oxidase subunit I (mtCOI) gene. The phylogenetic analysis among the obtained P. solenopsis mtCOI sequences with those already available in GenBank suggests Asian countries as a potential source of new introduction. This is the first record of P. solenopsis attacking tomato plants in Italy and may represent a potential threat for tomato production in Europe and nearby countries. For this reason, actions should be taken to avoid the uncontrolled spread of this alien species.

[1]  H. Jactel,et al.  Recent advances toward the sustainable management of invasive Xylosandrus ambrosia beetles , 2021, Journal of Pest Science.

[2]  M. Ricupero,et al.  Silica‐Microencapsulated Orange Oil for Sustainable Pest Control , 2021, Advanced Sustainable Systems.

[3]  S. Parnell,et al.  Commodity risk assessment of Ficus carica plants from Israel , 2021, EFSA journal. European Food Safety Authority.

[4]  I. Al-Jboory,et al.  First record of cotton mealybug, Phenacoccus solenopsis Tinsley 1898 (Hemiptera: Pseudococcidae), from Saudi Arabia , 2020 .

[5]  K. Haddi,et al.  First record of the invasive spotted wing Drosophila infesting berry crops in Africa , 2020 .

[6]  Sudhir Kumar,et al.  Molecular Evolutionary Genetics Analysis (MEGA) for macOS. , 2020, Molecular biology and evolution.

[7]  K. Wyckhuys,et al.  Global warming modifies long-distance migration of an agricultural insect pest , 2020, Journal of Pest Science.

[8]  M. Ulusoy,et al.  Mealybugs (Hemiptera: Coccomorpha: Pseudococcidae) on ornamental plants in eastern Mediterranean region, Turkey , 2020, Acta Horticulturae.

[9]  M. Jiang,et al.  Invasion biology of the cotton mealybug, Phenacoccus solenopsis Tinsley: Current knowledge and future directions , 2019, Journal of Integrative Agriculture.

[10]  N. Desneux,et al.  Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges , 2018, Journal of Pest Science.

[11]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[12]  Z. Mendel,et al.  The cotton mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in Israel: pest status, host plants and natural enemies , 2018, Phytoparasitica.

[13]  N. Desneux,et al.  Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future. , 2018, Annual review of entomology.

[14]  F. Porcelli,et al.  Aspidiotus bornmuelleri Lindinger, 1911, rev. comb. (Hemiptera: Coccomorpha: Diaspididae), a neglected endemic species from Macaronesia, with comments on the genus Cryptophyllaspis, and further notes on the scale insect fauna of Canary Islands, Spain , 2017 .

[15]  Douglass R. Miller,et al.  ScaleNet: a literature-based model of scale insect biology and systematics , 2016, Database J. Biol. Databases Curation.

[16]  H. Chen,et al.  Temperature- and Relative Humidity-Dependent Life History Traits of Phenacoccus solenopsis (Hemiptera: Pseudococcidae) on Hibiscus rosa-sinensis (Malvales: Malvaceae) , 2015, Environmental entomology.

[17]  I. Gavrilov-Zimin,et al.  Some additions to the mealybug fauna (Homoptera: Coccinea: Pseudococcidae) of the Canary Islands , 2015 .

[18]  Baoli Qiu,et al.  Genetic Record for a Recent Invasion of Phenacoccus solenopsis (Hemiptera: Pseudococcidae) in Asia , 2015, Environmental entomology.

[19]  B. B. Fand,et al.  The invasive mealybug Phenacoccus solenopsis Tinsley, a threat to tropical and subtropical agricultural and horticultural production systems - a review. , 2015 .

[20]  F. Wan,et al.  Analysis of expressed sequence tags (ESTs) from a normalized cDNA library and isolation of EST simple sequence repeats from the invasive cotton mealybug Phenacoccus solenopsis , 2015, Insect science.

[21]  L. Zeng,et al.  Homology difference analysis of invasive mealybug species Phenacoccus solenopsis Tinsley in Southern China with COI gene sequence variability , 2014, Bulletin of Entomological Research.

[22]  J. Zhao,et al.  Phenotypic variation and identification of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in China. , 2014, Zootaxa.

[23]  Vilayanoor Venkataraman Ramamurthy,et al.  Morphological and Molecular Studies on the Intraspecific Variations Between Populations of the Cotton Mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) , 2014, Entomological News.

[24]  M. Kaydan,et al.  New record of invasive mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) in Turkey , 2013 .

[25]  G. Siscaro,et al.  Tuta absoluta, a South American pest of tomato now in the EPPO region: biology, distribution and damage , 2012 .

[26]  Yijuan Xu,et al.  Does Mutualism Drive the Invasion of Two Alien Species? The Case of Solenopsis invicta and Phenacoccus solenopsis , 2012, PloS one.

[27]  T. Malausa,et al.  Identification of mealybug pest species (Hemiptera: Pseudococcidae) in Egypt and France, using a DNA barcoding approach , 2012, Bulletin of Entomological Research.

[28]  Runzhi Zhang,et al.  The potential distribution of an invasive mealybug Phenacoccus solenopsis and its threat to cotton in Asia , 2010 .

[29]  C. Hodgson,et al.  Phenacoccus solenopsis Tinsley (Sternorrhyncha: Coccoidea: Pseudococcidae), an invasive mealybug damaging cotton in Pakistan and India, with a discussion on seasonal morphological variation , 2008 .

[30]  A. Russo,et al.  Identification of Planococcus ficus and Planococcus citri (Hemiptera: Pseudococcidae) by PCR-RFLP of COI gene , 2008 .

[31]  Wolfgang Nentwig,et al.  Grasping at the routes of biological invasions: a framework for integrating pathways into policy , 2008 .

[32]  C. Szumik,et al.  Phenacoccinae de Centro y Sudamérica (Hemiptera: Coccoidea: Pseudococcidae): Sistemática y Filogenia , 2007 .

[33]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[34]  B. Crespi,et al.  Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers , 1994 .

[35]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[36]  M. Kimura.  A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[37]  J. Tinsley.  AN ANTS'-NEST COCCID FROM NEW MEXICO , 1898, The Canadian Entomologist.

[38]  N. A. El-Ghany,et al.  The cotton mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) as a new insect pest on tomato plants in Egypt , 2015 .

[39]  F. Porcelli,et al.  First record of Phenacoccus defectus in Italy, with comments on Phenacoccus solani and Phenacoccus solenopsis , 2013 .

[40]  D. Roy,et al.  Scales (Hemiptera, Superfamily Coccoidea). , 2010 .

[41]  J. Germain,et al.  Phenacoccus parvus Morrison et P. solenopsis Tinsley, deux Cochenilles nouvelles pour l'Egypte (Hemiptera, Pseudococcidae) , 2010, Bulletin de la Société entomologique de France.

[42]  Jeffrey S. Dukes,et al.  Impacts of Invasive Species on Ecosystem Services , 2008 .

[43]  Douglass R. Miller,et al.  Invasive species of mealybugs (Hemiptera: Pseudococcidae) and their threat to U.S. agriculture , 2002 .

[44]  D. Williams,et al.  Mealybugs of Central and South America. , 1992 .

[45]  D. Williams,et al.  The scale insects of the tropical South Pacific Region. Part 1. The armoured scales (Diaspididae). , 1988 .